- Likely native to Southeast Asia, sweet oranges are now commercially grown for fresh and processed (i.e., juice from-concentrate or not-from-concentrate) consumption.
- Throughout the global tropical and subtropical growing regions (top producers are Brazil and United States) worldwide production slightly down, but still topped 11.2 million tons in the United States during the 2012-2013 growing season.
- Orange juice has been implicated in 10 reported outbreaks, during which 810 persons became ill, in the United States from 1998 through 2012.
- Confirmed pathogenic agents reported to the United States National Outbreak Reporting System in orange juice associated outbreaks are limited to Salmonella (S. saintpaul, S. typhimurium, S. muenchen, S. anatum, and S. enteritidis) and Norwalk-like virus; however, suspected chemical or toxin contaminates have been reported.
The sweet orange (Citrus sinensis) is part of the genus Citrus that contains all citrus trees (e.g., oranges, grapefruits, lemons, limes, hybrids), which are interfertile. There are four distinct groups of sweet oranges including round oranges (most economically important), navel oranges, blood oranges, and acid-less oranges. While there is no universal agreement that the sour or bitter orange (Citrus aurantium) is a different species from C. sinensis, typically they are treated as separate species. While C. aurantium is produced and harvested in a similar manner as the sweet orange, uses differ. This article will focus on understanding the production process and health implications surrounding C. sinensis.
The C. sinensis tree, which is typically 22 to 30 feet (7 to 10 meters) in a pruned commercial grove, have 3 to 5 inch (8 to 13cm) long dark green evergreen leaves that last two to three years. The blade of the sweet orange leaf has a round base with pointed apex and typically has a small spine at the axil.
The flower of the sweet orange is white and self-pollinating; although, bees do assist in pollination. Seedless fruit cultivars are produced by flowers with little to no pollen or fertile ovules.
The sweet orange fruit is a spherical or oblong hesperidium that ranges in size from 2-1/2 to 4 inches (6 to 10cm) in diameter. The surface of the peel can be smooth to rough with pockmarks. The peel thickness ranges between a tangerine and grapefruit, and adheres tightly to the flesh of the fruit, except in navel cultivars.
Sweet oranges were established in Florida between 1513 and 1565 near St. Augustine, with seeds having been imported from Europe. Commercial orange groves in Florida have continually been pushed further south to avoid fruit killing and impact freezes (kills juvenile and mature trees), most recently during December 1989. In the United States, Florida was the top producer of oranges for juicing, producing 6.3 million tons of oranges (88.9%). The next top producers in this category were California (8.7%), Texas (1.9%), and Arizona (0.4%) during the 2012-2013 growing season. In the same growing season, California was the top producer of oranges for fresh consumption, producing 3.2 million tons (76.6%), followed by Florida (17.6%), Texas (4.5%), and Arizona (1.3%).
Common Sweet Orange Varieties
A quick identification guide to the most common commercially grown orange varieties is presented below.,
Round Oranges are able to be harvested throughout the potential 10 month Florida orange harvest season by growing ‘early’, ‘mid-season’, and ‘late’ varietals. Hamlin, Pineapple, and Valencia are the principal varietals grown in their respective season in Florida. Round oranges are primarily processed (i.e., juice from-concentrate or not-from-concentrate).
The Hamlin orange is a varietal with ancestral roots linked to a fortuitous seed planting in the grove of namesake A.C. Hamlin near DeLand, Florida in 1879. Freezes during the 1980s allowed the Hamlin to replace the Parson-Brown as the dominant early-season orange varietal in Florida.
With the harvest season beginning in October before the chance of a freeze of a commercially seedless fruit (0 to 6 seeds per fruit) and cold-tolerance of the tree combines to make the Hamlin very popular in Florida. The Hamlin fruit is 2-3/4 to 3 inches in diameter with a smooth, thin, and poorly colored peel. While the Hamlin is a heavy producer, consumers find the juice color to be poor. Therefore, typical commercial practice is to blend the juice with other varietals during production.
The Pineapple orange, named for the aromatic fragrance of the fruit, traces it’s roots back to a grove in Citra, Florida planted from seed in 1860. Known for it’s excellent juice color and quality, the Pineapple has a harvest season from December until February and is the dominant mid-season Florida varietal. The fruit is 2-3/4 to 3 inches in diameter and slightly flattened on each end. The peel, typically orange but can develop an appealing red-orange color if nights drop below 55 degree Fahrenheit, is smooth and thicker than a Hamlin. With counts ranging from 15 to 25 per fruit, the Pineapple is a seedy varietal and as a result is used almost exclusively in the processed market.
Used in both the processed and fresh markets, the Valencia orange is the most widely grown sweet orange varietal in the United States and the world. While the economically important varietal has a disputed past, first accounts of importation to Florida occurred in 1877.
The Valencia is Florida’s leading late-season varietal with the harvest season beginning in March and extending into June. Farmers have two unique challenges when growing Valencia oranges including fruits developing on the trees during the winter months (potential freeze damage) and the tree typically produces two crops past flower bloom. The fruit is 2-3/4 to 3 inches in diameter, commercially seedless (0 to 6 seeds per fruit), and notoriously juicy. The peel is thin and will remain green without cool nights even when the fruit is ripe. As a result, fruit bound for the fresh market may be treated with ethylene gas to turn the peel an attractive orange color consumers expect.
A naturally occurring mutation is likely to have occurred in Brazil prior to the introduction of the Navel orange to the United States in 1870. This mutation provides the varietal namesake due to a unique second and sometimes tertiary embryo growth at the fruit apex, which is similar in appearance to the human navel. However, the mutation is unstable making selection of trees from a nursery of particular importance for growers.
The Navel tree produces no pollen resulting in a commercially seedless (0 to 6 seeds) fruit. Species propagation is exclusively through budding and cloning. One of the original two parent Navel trees that all Washington Navels are descendants from was imported to Riverside, California in 1873 and is still producing fruit today. The Washington is second only to the Valencia among Sweet Orange varietal production both in the United States and worldwide. Unlike the Valencia, Navel oranges do not grow well in tropical climates; however, the sub-tropical climates of both Florida and Brazil produce quality fruit.
The size among the over 50 Navel orange varieties can vary, but typically are on the larger side (3 to 3-1/2 inches in diameter) of the spectrum between tangerines and grapefruit. With a yellow to orange colored pebbled peel that is easy to peel and fruit with low acid concentration that is easily sectioned, the Navel is excellent for eating fresh. The juice is slightly bitter making the fruit less suitable for juicing. The Navel is harvested in Florida from October to January; fruit at the end of the season can taste and appear dried out.
Cara Cara, or Red Navel, was discovered in Venezuela in 1976 with production today based in California, Venezuela, and South Africa. Harvest seasons of the Cara Cara typically lead to arrival from South Africa in August, Venezuela in October, and California in November.
The Blood orange is the product of a natural mutation in the sweet orange and is from the Mediterranean basin where it has been cultivated since the 15th century, especially in Spain and Italy.
Smaller in size, the Blood orange (e.g., Moro, Ruby, Tarocco) has a diameter of 2-1/2 to 2-3/4 inches and is a pink blush fruit that can be oval, round, or oblate in shape. The varietal is known for its unique sweet flavor that is similar in taste and appearance to a Valencia, but with a deep red streaky pigment in the flesh. The deep red color is from increased concentrations of the pigment anthocyanin, which increases when growing conditions are cooler. As a result, Blood oranges grown in Florida typically do not have a deep red color due to the warm, humid climate. The fruit contains few seeds, ranging from four to ten.
Acid-less oranges (e.g., Lima) tend to be early-season varietals with remarkably little flavor. While grown for local consumption in the Mediterranean basin, Brazil, Egypt, Mexico, and Spain, due to the very low acid concentration these varietals are unable to be transported widely as they readily spoil.
From 1998 to 2014, there have been 11 outbreaks and 838 illnesses associated with oranges in the United States, with five outbreaks occurring in Florida. Of these outbreaks, four were caused by Salmonella, two were caused by norovirus, two were caused by a chemical/toxin, and three were of unknown etiology. Outbreaks associated with oranges and orange juice have led to various policy changes and recalls.
Three outbreaks have been associated with orange juice served at hotel breakfasts. In 1944, an outbreak of Salmonella Typhi in Ohio caused illness in 18 individuals. In 1989, an outbreak of Salmonella Typhi in a New York hotel caused illness in 70 individuals. Salmonella Typhi is the pathogen that causes typhoid fever; both outbreaks were attributed to an asymptomatic food handler preparing breakfast for hotel guests. In 2004, an outbreak associated with the consumption of unpasteurized orange juice served at a hotel in Egypt was the source of a Hepatitis A outbreak, causing 351 individuals to fall ill across nine countries. An investigation of the orange juice processing facility indicated that working conditions were unsanitary and the orange juice was not properly heat treated. Results concluded the presence of a dose-response relationship; the number of days of orange juice consumption was directly proportional to infection.
Multiple outbreaks associated with unpasteurized orange juice have been linked to Salmonella. In 1995, unpasteurized orange juice served in a large Florida theme park caused 72 illnesses across 21 states. This multi-state outbreak of Salmonella Gaminara was linked to contamination during processing. In response to this event, the theme park decided it would only sell pasteurized orange juice and the Florida Department of Citrus issued new regulations for the production of unpasteurized fresh squeezed orange juice. In 1999, separate clusters of Salmonella Muenchen were identified by the Washington state health department and the Oregon Health Division., Further investigation revealed a multi-state outbreak of 207 confirmed cases across a total of 15 states and two Canadian provinces., The source was determined as unpasteurized orange juice from Sun Orchard that was distributed under multiple brand names., Sun Orchard voluntarily issued a recall in response to the outbreak., In 2005, a multi-state outbreak of 152 cases across 23 states was caused by Salmonella Saintpaul and Typhimurium. Both pathogens were found in unpasteurized orange juice from the same company. Although the source of contamination was not identified, noncompliance with the juice Hazard Analysis and Critical Control Point (HACCP) regulation likely contributed to this outbreak.
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The juvenile period, where there is no fruit production, of a sweet orange tree grown from seed is approximately 8 to 12 years. Cultivars have reduced this time period to approximately 3 years by grafting a bud from the desired fruit tree (scion) onto a stem of a young seedling (rootstock) grown in a nursery. Rootstock is selected based on cold tolerance, pest resistance, and influence on the productivity, quality, and vigor of the type of scion attached.
Orange groves are laid out in rows to maximize space, sun penetration, and harvest efficiency. As land and water have become more scarce in Florida, the within-row spacing of orange grove trees has decreased from 25 feet to 15 feet. The between-row spacing has remained constant overtime at 25 feet. Herbicide is applied under the planted tree to reduce competition for nutrients, reduce pest habitat, and allow free percolation of water and applied nutrients to the root zone. The middle of grove rows are allowed to grow over and are mowed as needed.
Sweet orange trees are trimmed with large mechanical hedgers after the seasons crop has been harvest. Trimmings are mulched into the middle of grove rows.
Soil and Amendments
Florida soil is primarily composed of a gray fine sand called ‘myakka’. Myakka is great for sweet orange growing as they require a well-drained soil with adequate depth avoiding a high water table. On average, Florida’s soil pH is 6.1, but locally the parent material determines the soil pH. For example, soil from under pine flatwoods is very acidic, but in parts of Central Florida and South Florida the high limestone bedrock (pH 7.8 to 8.1), which is composed of alkaline calcium carbonate, increases the soil pH. In a commercial sweet orange grove, testing the soil, typically in the fall, to adjust salinity and pH (between 6 and 7) is necessary for optimum growth; however, testing of the leaves provides more reliable information on nutrient deficiencies.,
The nutrient limited soils of Florida need to be supplemented with the 14 elements that are needed for optimal orange growth are calcium (Ca), magnesium (Mg), sulfur (S), iron (Fe), zinc (Zn), manganese (Mn), boron (B), copper (Cu), molybdenum (Mo), chlorine (Cl), nickel (Ni), and the big three being nitrogen (N), phosphorus (P), and potassium (K). In Florida, fertilizer is usually applied 3 to 4 times per year, but use of biannual slow release dry fertilizer has recently become more economical. Fertilizer applied by fertigation has become more popular (typically nitrogen and potassium), but tractor and aerial foliar spraying is also commonly employed in Florida. Use of treated biosoilds can reduce potential contamination events.,
Gravity irrigation, also known as surface or flood irrigation, is when water is allowed to run through channels dug through the grove near the tree root zone. This method has become less popular due to the high water usage and need to maintain water channels every two to three years. Drip irrigation, allows the slow release of water through a hose network with releases near the tree root zone that can be laid on the surface or buried underground. This method is preferred when using reclaimed water as potential biological contamination does not come into contact with the fruit. Overhead sprinklers, require high pressure systems using uncontaminated water due to contact with the fruit. The most popular system used today in Florida is micro-irrigation systems that consist of a small, low pressure hose system with misters above the tree root zone.
Freeze and Frost Protection
A radiation frost occurs when an inversion layer develops on a clear night with calm winds and can damage flowers preventing fruit development. When the temperature falls below 28 degrees Fahrenheit for at least four hours fruit can experience freeze damage. Freeze damaged fruit can still be harvested for juicing. The greatest threat to orange groves occurs when temperatures drop to extreme lows (four hours at 20 degrees Fahrenheit) or just below freezing for extended periods of time (28 degrees Fahrenheit for 12 continuous hours) which causes ice formation in the tree tissue, potentially causing limb or tree death.
Smudge pots, rarely used today, are filled with oil and burned throughout the orange groves to raise the temperature enough to prevent extensive crop damage. A piped fuel heater system with oil, natural gas, or propane can also be used. When a radiation frost with calm wind is predicted, windmills can be used to raise the temperature by disruption of an inversion layer. Helicopters have also be used for the same purpose.
The most popular method for frost and freeze protection is irrigation. In the irrigation method, water is sprayed on or under the tree canopy. As the water cools latent energy is released as heat creating a micro-climate. Once the irrigation method is started, water spraying cannot be stopped until temperatures elevate to where the ice is loose and melting. This preventative method is typically used with under-canopy or micro-irrigation systems due to potential ice buildup and limb breakage when over-canopy sprinklers are used. Advantages of the irrigation method are in the cost savings as water is cheaper than fuel and the same system can be used for drought prevention, fertilizer application, and some pest control.
The US Environmental Protection Agency sets Maximum Residue Levels for pesticides on fresh fruit. Over 90% of Florida oranges are grown to meet these standards even though the majority of Florida oranges are used for juice production
In 2009, approximately 93 percent of Florida oranges were treated with at least one type of insecticide, but standard applications range from 6 to 12 times per year. Commonly used insecticides in Florida are abamectin, aldicarb, carbaryl, dimethoate, fenpropathrin, imidacloprid, and petroleum oil.
Most common citrus diseases in Florida are citrus canker, citrus black spot, Phytophthora crown/foot/root rots, brown rot, greasy spot, melanose, postbloom fruit drop, and citrus scab. However, citrus greening is the most serious citrus disease in Florida and worldwide.
Huanglongbing (Citrus Greening)
Huanglongbing (HLB), meaning “yellow shoot disease” and named for one of the disease manifestations, is suspected to be caused by the bacterium Candidatus liberibacter asiaticus. Having already impacted the citrus crops in Africa, Asia, Indian subcontinent, and Arabic peninsula, HLB was discovered in Florida in August 2005. HLB is of significant concern as it can impact all citrus. HLB is now in all Florida counties with commercial citrus production. Symptoms of HLB include yellowing of leaves, foliage drop, lopsided and bitter fruit, fruit drop, and tree stunting and death.
In 1998 the Asian citrus psyllid (Diaphorina citri Kuwayama), the vector of HLB, was identified in Florida. While unimposing at only 3 to 4 millimeters long, during its 15 to 47 day life cycle the female can lay upwards of 800 eggs. This equates to approximately 9 to 10 generations a year. HLB is transmitted when the psyllid (adult or nymph) feeds on a diseased tree. The disease needs a 21 day incubation period, but is then transmittable for life when the infected psyllid feeds on the leaves of an uninfected tree. Vertical transmission has not been indicated.
Management of the HLB revolves around reducing psyllid populations, preventing their geographical spread, and ensuring groves receive proper nutrition. Nutrient foliar spraying has been used to keep diseased trees productive with some success. Currently no treatment is available to treat HLB infected trees. As efforts mount, public health professionals should stay informed of new methods used to combat HLB.
Sweet oranges once picked do not ripen further; therefore, farmers must closely monitor their crop for peak maturity. An orange picked before maturity will tend to shrivel and are more likely to incur mechanical damage during processing. An orange picked after peak maturity will rapidly become soft and insipid. To assist in this delicate decision, farmers rely on visual inspection, taste testing, and laboratory analysis where a ‘soluble solid (or brix) / acid’ ratio is calculated. The minimum requirement for USDA Grade A canned orange juice is 10.5 to 1 brix/acid ratio.
Some farmers use an abscission agent (e.g., 5-chloro-3-methyl-5-nitro-1H-pyrazole (CMNP) to loosen the fruits attachment to the tree, which improves efficiency of both manual and mechanical harvesting.
The majority of Florida oranges are picked by hand with workers climbing ladders with shoulder sacks that are then emptied in 900 pound field boxes. Field boxes are transported by a specialized truck called a ‘goat’ to an open tractor-trailer, which can hold roughly 45,000 pounds of oranges, for transport to the packing or processing facility.
Finding enough workers to manually harvest the 146,600 acres of Florida orange groves in 2013 makes mechanical harvesting an attractive option. However, a significant upfront investment and concerns over tree damage to already very stressed orange trees in Florida from citrus greening has kept use of mechanical harvesting to a minimum.
Processing, Packing, and Storage
Oranges grown in a climate where the nights are not cool tend to produce oranges with some green color still in the rind even though the fruit is ripe. Some producers of oranges for fresh consumption will treat these oranges with ethylene gas. The treatment will not further ripen the orange, but will help de-green the fruit (i.e., remove the chlorophyll); however, this process may increase decay rates. A typical de-greening method may use 3-5 parts per million (ppm) ethylene under ideal conditions.
Upon arrival at the packing plant, oranges are loaded onto conveyor belts and sent through soaking and pressure washing system. Washed oranges are then either mechanically or manually sorted to remove fruit with physical or ascetic defects. Rejected oranges are sent to be made into orange juice. A fungicide and edible polyethylene wax are then spayed onto the orange before final packaging for fresh consumption.
Fresh oranges have an optimal holding temperature of 32 to 34 degrees Fahrenheit to maximize duration of shelf life. Moisture loss in the peel and pulp is the limiting factor in storage duration.
Oranges arriving at the processing facility are cleaned, washed, and juice extracted on high throughput mechanical squeezers. The orange peel is pressed to extract the oil, used later in processing for flavoring. The pulp is then filtered from the juice and both separately pasteurized. The pasteurized juice can be stored in large tanks to allow for blending of different varietals to create a consistent product. During final processing, if orange juice with pulp is desired, pulp is added back into the juice along with peel oil for flavoring. The juice is then aseptically filled into sterile containers.
Unpasteurized orange juice undergoes a similar process through the extraction step, but receives little process beyond some filtering before final packaging and distribution. The final product must be continually refrigerated and typically has a short shelf-life.
Frozen from Concentrate
After unloading from the delivery tractor-trailer, the fruit is cleaned, washed, and juice extracted. Approximately 50% of the weight of the orange is juice. The peel of the orange is pressed for the oil, which will be added back later in the process to improve taste and smell of the frozen concentrate. The juice is filtered to remove seeds and large pieces of pulp, then pasteurized to inactivate enzymes and biological contaminates. A high heat vacuum evaporator is used to quickly remove excess water. The concentrate can be frozen in tanks until needed.
During the final processing steps, the frozen concentrate is combined with pasteurized orange peel oil and juice to add flavor back that was taken out during the evaporation step. The final product is filled into sterile packaging. The minimum brix of the final product is 41.8 degrees, which will be diluted out to the approximate brix percent observed in freshly squeezed orange juice when the consumer adds the recommended quantity of water.
The peel of retail purchased fresh oranges, while used as a flavor enhancer in home cooking, are not usually consumed, but removed and discarded, in effect reducing the risk of illness from any potential exterior biological contamination. Public health professionals investigating an outbreak with possible fresh orange involvement should consider contamination by a food worker during hand slicing or peeling.
Fresh and frozen from concentrate orange juice has been commonly thought to be safe for consumption solely based on a low pH; however, numerous outbreaks have shown that orange juice can harbor and transmit infectious pathogens.
From 1922 through 2010, 14 outbreaks associated with consumption of orange juice were reported worldwide. Of these, 9 (64%) were from unpasteurized orange juice, 4 (29%) from frozen from concentrate, and 1 (7%) was unspecified. All reported outbreaks linked with unpasteurized orange juice were associated with either retail or food service establishments; whereas; outbreaks associated with consumption of frozen from concentrate orange juice were in hospitals (2, 50%), a hotel (1, 25%), and at a sporting event (1, 25%). Pathogens identified in unpasteurized orange juice outbreaks were predominately Salmonella (S. typhimurium, S. saintpaul, S. enteritidis, S. anatum, S. menchen, S. gaminara, S. hartford, S. rubislaw), but also included enterotoxigenic E. coli, Shigella flexneri, and a suspected virus. Frozen from concentrate orange juice contaminates identified in outbreaks include Salmonella typhi, Hepatitis A, and a suspected Norwalk-like virus.
The inherent nature of manufacturing orange juice provides more opportunity for a single contaminated orange to cause an outbreak, compared to oranges consumed fresh, as the juice from thousands of oranges is combined before distribution and has more steps in the manufacturing process. Due to climatic variations that affect the fruit or manufacturer processing techniques, the pH of orange juice may rise above the normally observed range (3.6 to 4.3), which can permit pathogen growth. Also, some pathogens in orange juice, even at normally observed pH levels, will only be inhibited from reproductive growth and will remain infectious. As a result, a risk for illness from unpasteurized orange juice persists.
The incorporation of pasteurization into the production process has made fresh and frozen from concentrate orange juice safe to consume. However, a risk remains in drinking unpasteurized orange juice as contamination can still occur by food handlers.
A selection of outbreak reports associated with unpasteurized orange juice are provided below that highlight some of the principle food safety issues that have led to significant human illness.
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Fresh sweet oranges are a low calorie (60 calories per 1 medium peeled orange), nutritious source of vitamin C (120% Daily Value (DV), fiber (12% DV), vitamin A (6% DV), and calcium (6% DV). The fresh fruit contains no saturated fats or cholesterol, but has high pectin concentrations, a beneficial dietary fiber. Orange juice is an excellent source for daily nutrition, however, consumers should read orange juice nutrition labels to observe a recommended severing size, as like all fruit juices, orange juice is calorie rich.